Arabidopsis SUMO protease ASP1 positively regulates flowering time partially through regulating FLC stability

Abstract

The initiation of flowering is tightly regulated by the endogenous and environment signals, which is crucial for the reproductive success of flowering plants. It is well known that autonomous and vernalization pathways repress transcription of FLOWERING LOCUS C (FLC), a focal floral repressor, but how its protein stability is regulated remains largely unknown. Here, we found that mutations in a novel Arabidopsis SUMO protease 1 (ASP1) resulted in a strong late-flowering phenotype under long-days, but to a lesser extent under short-days. ASP1 localizes in the nucleus and exhibited a SUMO protease activity in vitro and in vivo. The conserved Cys-577 in ASP1 is critical for its enzymatic activity, as well as its physiological function in the regulation of flowering time. Genetic and gene expression analyses demonstrated that ASP1 promotes transcription of positive regulators of flowering, such as FT, SOC1 and FD, and may function in both CO-dependent photoperiod pathway and FLC-dependent pathways. Although the transcription level of FLC was not affected in the loss-of-function asp1 mutant, the protein stability of FLC was increased in the asp1 mutant. Taken together, this study identified a novel bona fide SUMO protease, ASP1, which positively regulates transition to flowering at least partly by repressing FLC protein stability.

Exploiting protein modification systems to boost crop productivity: SUMO proteases in focus

“…As protein and/or transcript levels of almost all characterized ULP SUMO proteases (the northern blot performed in esd4 mutants is inconclusive) are known to be elevated in developing flowers (Murtas et al , 2003; Hermkes et al , 2011; Castro et al , 2016; Kong et al , 2017), we suspect the ULP mutants may be harbouring undiscovered floral phenotypes. For example, esd4 mutants exhibit deformed and irregularly placed siliques (Reeves, 2002) reminiscent of sum1-1 amiR-SUM2 SUM1/2 knockdown plants (van den Burg et al , 2010), which may be caused by defective flower or seed formation earlier in development.…”

“…Meanwhile, esd4 , ots1/2 , and spf1 mutants exhibit higher levels of SUMO conjugation in non-stressed conditions (Conti et al , 2008; Hermkes et al , 2011; Liu et al , 2017), while the ability to recover from stress-induced SUMO conjugate accumulation was shown to be compromised in spf1 mutants (Kong et al , 2017). Phenotypically, ots1/2 mutants are more sensitive to salt, osmotic stress, and abscisic acid (Conti et al , 2008; Castro et al , 2016; Srivastava et al , 2017).…”

“…They are cysteine proteases, characterized by a conserved H–D–C catalytic triad (Kurepa et al , 2003). A consensus group of seven ULPs has been identified in Arabidopsis, of which six have been characterized (Murtas et al , 2003; Novatchkova et al , 2004; Conti et al , 2008; Hermkes et al , 2011; Kong et al , 2017; Liu et al , 2017). The observation that substantially more ULPs than E3 ligases are present in Arabidopsis has led to the hypothesis that specificity in the SUMO system may also be conferred by deSUMOylation (Yates et al , 2016).…”

Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development

“…ULPs fall into two large groups (ULP1s and ULP2s), by homology to yeast ScULP1 and ScULP2. The Arabidopsis genome includes eight predicted ULPs, six of which have been shown to function as SUMO proteases in vitro (Chosed et al , 2006; Colby et al , 2006; Conti et al , 2008; Novatchkova et al , 2012; Kong et al , 2017; Liu et al , 2017 a ). Each of these ULPs is likely to contribute individually to specific functions within the plant, judging from the functional characterizations available to date.…”

“…OTS1 and OTS2 act redundantly in flowering transition, plant growth, and photomorphogenesis, as well as in pathogen defence, and salt and osmotic stress responses (Conti et al , 2008, 2014; Sadanandom et al , 2015; Bailey et al , 2016; Castro et al , 2016). The function of SPF1 (also designated ASP1) and SPF2 has been recently associated with the control of flowering time, and gamete and embryo development (Kong et al , 2017; Liu et al , 2017 a ). …”